Morphological constraints on changing avian migration phenology.

Many organisms at northern latitudes have responded to climate warming by advancing their spring phenology. Birds are known to show earlier timing of spring migration and reproduction in response to warmer springs. However, species show heterogeneous phenological responses to climate warming, with those that have not advanced or have delayed migration phenology experiencing population declines. Although some traits (such as migration distance) partly explain heterogeneity in phenological responses, the factors affecting interspecies differences in the responsiveness to climate warming have yet to be fully explored. In this comparative study, we investigate whether variation in wing aspect ratio (reflecting relative wing narrowness), an ecomorphological trait that is strongly associated with flight efficiency and migratory behaviour, affects the ability to advance timing of spring migration during 1960-2006 in a set of 80 European migratory bird species. Species with larger aspect ratio (longer and narrower wings) showed smaller advancement of timing of spring migration compared to species with smaller aspect ratio (shorter and wider wings) while controlling for phylogeny, migration distance and other life-history traits. In turn, migration distance positively predicted aspect ratio across species. Hence, species that are better adapted to migration appear to be more constrained in responding phenologically to rapid climate warming by advancing timing of spring migration. Our findings corroborate the idea that aspect ratio is a major evolutionary correlate of migration, and suggest that selection for energetically efficient flights, as reflected by high aspect ratio, may hinder phenotypically plastic/microevolutionary adjustments of migration phenology to ongoing climatic changes.

Sex allocation according to multiple sexually dimorphic traits of both parents in the barn swallow (Hirundo rustica).

Parents should differentially invest in sons or daughters depending on the sex-specific fitness returns from male and female offspring. In species with sexually selected heritable male characters, highly ornamented fathers should overproduce sons, which will be more sexually attractive than sons of less ornamented fathers. Because of genetic correlations between the sexes, females that express traits which are under selection in males should also overproduce sons. However, sex allocation strategies may consist in reaction norms leading to spatiotemporal variation in the association between offspring sex ratio (SR) and parental phenotype. We analysed offspring SR in barn swallows (Hirundo rustica) over 8 years in relation to two sexually dimorphic traits: tail length and melanin-based ventral plumage coloration. The proportion of sons increased with maternal plumage darkness and paternal tail length, consistently with sexual dimorphism in these traits. The size of the effect of these parental traits on SR was large compared to other studies of offspring SR in birds. Barn swallows thus manipulate offspring SR to overproduce 'sexy sons' and potentially to mitigate the costs of intralocus sexually antagonistic selection. Interannual variation in the relationships between offspring SR and parental traits was observed which may suggest phenotypic plasticity in sex allocation and provides a proximate explanation for inconsistent results of studies of sex allocation in relation to sexual ornamentation in birds.

With a little help from my kin: barn swallow nestlings modulate solicitation of parental care according to nestmates' need.

In altricial species, offspring competing for access to limiting parental resources (e.g. food) are selected to achieve an optimal balance between the costs of scrambling for food, the benefits of being fed and the indirect costs of subtracting food to relatives. As the marginal benefits of acquiring additional food decrease with decreasing levels of need, satiated offspring should be prone to favour access to food by their needy kin, thus enhancing their own indirect fitness, while concomitantly reducing costs of harsh competition with hungry broodmates. We tested this prediction in feeding trials of barn swallow (Hirundo rustica) nestlings by comparing begging behaviour and food intake of two similar-sized nestmates, one of which was food-deprived (FD). Non-food-deprived (NFD) offspring modulated begging intensity depending on their nestmate's need: when competing with FD nestmates, NFD nestlings reduced both the intensity and frequency of begging displays compared to themselves in the control trial before food deprivation. Hence, NFD nestlings reduced their competitiveness to the advantage of FD nestmates, which obtained more feedings and showed a threefold larger increase in body mass. Moderation of individual selfishness can therefore be adaptive in the presence of a needier kin, because the indirect fitness benefits of promoting its condition can outweigh the costs of forgoing being fed, and because it limits the cost of begging escalation against a vigorous competitor.

MHC genotype predicts mate choice in the ring-necked pheasant Phasianus colchicus.

Females of several vertebrate species selectively mate with males on the basis of the major histocompatibility complex (MHC) genes. As androgen-mediated maternal effects have long-lasting consequences for the adult phenotype, both mating and reproductive success may depend on the combined effect of MHC genotype and exposure to androgens during early ontogeny. We studied how MHC-based mate choice in ring-necked pheasants (Phasianus colchicus) was influenced by an experimental in ovo testosterone (T) increase. There was no conclusive evidence of in ovo T treatment differentially affecting mate choice in relation to MHC genotype. However, females avoided mating with males with a wholly different MHC genotype compared with males sharing at least one MHC allele. Females also tended to avoid mating with MHC-identical males, though not significantly so. These findings suggest that female pheasants preferred males with intermediate MHC dissimilarity. Male MHC heterozygosity or diversity did not predict the expression of ornaments or male dominance rank. Thus, MHC-based mating preferences in the ring-necked pheasant do not seem to be mediated by ornaments' expression and may have evolved mainly to reduce the costs of high heterozygosity at MHC loci for the progeny, such as increased risk of autoimmune diseases or disruption of coadapted gene pools.

Rapid change in host use of the common cuckoo Cuculus canorus linked to climate change.

Parasites require synchrony with their hosts so if host timing changes with climate change, some parasites may decline and eventually go extinct. Residents and short-distance migrant hosts of the brood parasitic common cuckoo, Cuculus canorus, have advanced their phenology in response to climate change more than long-distance migrants, including the cuckoo itself. Because different parts of Europe show different degrees of climate change, we predicted that use of residents or short-distance migrants as hosts should have declined in areas with greater increase in spring temperature. Comparing relative frequency of parasitism of the two host categories in 23 European countries before and after 1990, when spring temperatures in many areas had started to increase, we found that relative parasitism of residents and short-distance migrants decreased. This change in host use was positively related to increase in spring temperature, consistent with the prediction that relative change in phenology for different migrant classes drives host-use patterns. These findings are consistent with the hypothesis that climate change affects the relative abundance of different host races of the common cuckoo.

Sex-related variation in migration phenology in relation to sexual dimorphism: a test of competing hypotheses for the evolution of protandry.

Timing of arrival/emergence to the breeding grounds is under contrasting natural and sexual selection pressures. Because of differences in sex roles and physiology, the balance between these pressures on either sex may differ, leading to earlier male (protandry) or female (protogyny) arrival. We test several competing hypotheses for the evolution of protandry using migration data for 22 bird species, including for the first time several monochromatic ones where sexual selection is supposedly less intense. Across species, protandry positively covaried with sexual size dimorphism but not with dichromatism. Within species, there was weak evidence that males migrate earlier because, being larger, they are less susceptible to adverse conditions. Our results do not support the 'rank advantage' and the 'differential susceptibility' hypotheses, nor the 'mate opportunity' hypothesis, which predicts covariation of protandry with dichromatism. Conversely, they are compatible with 'mate choice' arguments, whereby females use condition-dependent arrival date to assess mate quality.

Maternal allocation strategies and differential effects of yolk carotenoids on the phenotype and viability of yellow-legged gull (Larus michahellis) chicks in relation to sex and laying order.

Egg quality may mediate maternal allocation strategies according to progeny sex. In vertebrates, carotenoids have important physiological roles during embryonic and post-natal life, but the consequences of variation in yolk carotenoids for offspring phenotype in oviparous species are largely unknown. In yellow-legged gulls, yolk carotenoids did not vary with embryo sex in combination with egg laying date, order and mass. Yolk lutein supplementation enhanced the growth of sons from first eggs but depressed that of sons from last eggs, enhanced survival of daughters late in the season, and promoted immunity of male chicks and chicks from small eggs. Lack of variation in egg carotenoids in relation to sex and egg features, and the contrasting effects of lutein on sons and daughters, do not support the hypothesis of optimal sex-related egg carotenoid allocation. Carotenoids transferred to the eggs may rather result from a trade-off between opposing effects on sons or daughters.

Increased egg estradiol concentration feminizes digit ratios of male pheasants (Phasianus colchicus).

The length ratio between individual digits differs between males and females in humans, other mammals, lizards, and one bird species. Sexual dimorphism in digit ratios and variation among individuals of the same sex may depend on differential exposure to androgens and estrogens during embryonic life. Organizational effects of sex hormones could cause the observed correlations between digit ratios and diverse phenotypic traits in humans. However, no study has investigated experimentally the effect of prenatal estrogens on digit ratios. We analyzed the effect of estradiol injection in ring-necked pheasant (Phasianus colchicus) eggs on digit ratios. Males from control eggs had higher ratios between the second or third and the fourth digit of the right foot compared to females. Estradiol-treated eggs produced males with lower (feminized) right foot second to fourth digit ratio. Thus, we provided the first experimental evidence that prenatal exposure to physiologically high estrogen levels affects bird digit ratios.

Early maternal, genetic and environmental components of antioxidant protection, morphology and immunity of yellow-legged gull (Larus michahellis) chicks.

Maternal effects mediated by egg quality are important sources of offspring phenotypic variation and can influence the course of evolutionary processes. Mothers allocate to the eggs diverse antioxidants that protect the embryo from oxidative stress. In the yellow-legged gull (Larus michahellis), yolk antioxidant capacity varied markedly among clutches and declined considerably with egg laying date. Analysis of bioptic yolk samples from clutches that were subsequently partially cross-fostered revealed a positive effect of yolk antioxidant capacity on embryonic development and chick growth, but not on immunity and begging behaviour, while controlling for parentage and common environment effects. Chick plasma antioxidant capacity varied according to rearing environment, after statistically partitioning out maternal influences mediated by egg quality. Thus, the results of this study indicate that egg antioxidants are important mediators of maternal effects also in wild bird populations, especially during the critical early post-hatching phase.

Colour polymorphism in birds: causes and functions.

We studied polymorphism in all species of birds that are presently known to show intraspecific variation in plumage colour. At least three main mechanisms have been put forward to explain the maintenance of polymorphism: apostatic, disruptive and sexual selection. All of them make partly different predictions. Our aims were to investigate evolutionary causes and adaptive functions of colour polymorphism by taking into account a number of ecological and morphological features of polymorphic species. Overall, we found 334 species showing colour polymorphism, which is 3.5% of all bird species. The occurrence of colour polymorphism was very high in Strigiformes, Ciconiiformes, Cuculiformes and Galliformes. Phylogenetically corrected analysis using independent contrasts revealed that colour polymorphism was maximally expressed in species showing a daily activity rhythm extended to day/night, living in both open and closed habitats. All these findings support the hypothesis that colour polymorphism probably evolved under selective pressures linked to bird detectability as affected by variable light conditions during activity period. Thus, we conclude that selective agents may be prey, predators and competitors, and that colour polymorphism in birds may be maintained by disruptive selection.

Humoral immune response in relation to senescence, sex and sexual ornamentation in the barn swallow (Hirundo rustica).

Performance of animals may decline with age. The effects of senescence, however, may differ between the sexes because of differences in physiology and behaviour. Acquired immunity provides hosts with efficient mechanisms of anti-parasite defence, but the effect of senescence on immunocompetence has never been studied in natural populations. In the barn swallow (Hirundo rustica), primary antibody response to an antigen during one breeding season declined with age in females, while secondary response during the following breeding season declined with age in both sexes. Parasite-mediated sexual selection theory posits that male secondary sexual characters reveal resistance to parasites. Males with large tail ornaments had stronger primary response, retained larger antibody levels until the following year, but did not differ in secondary response compared with short-tailed males, as predicted if ornamentation reflects resistance to parasites. This is the first study showing that immunocompetence declines with age in any vertebrate under natural conditions.